RESTORATION OF EUTROPHIC LAKES

Development of Lake Vesijarvi through four decadesof remediation efforts

Kalevi Salonen . Jouko Sarvala . Jukka Horppila . Juha Keto .

Ismo Malin . Tommi Malinen . Juha Niemisto . Jukka Ruuhijarvi

Received: 3 October 2019 / Revised: 7 June 2020 / Accepted: 17 June 2020

� The Author(s) 2020

Abstract The diversion of sewage inputs in the mid-

1970s led to an order of magnitude reduction in

nutrient loading to Lake Vesijarvi, southern Finland.

After the diversion, nutrient concentrations declined,

consistent with a simple dilution model, and by the

mid-1990s the chlorophyll concentration was reduced

by 80%. The favourable development was supported

by a 5-year mass removal of planktivorous and

benthivorous fish and the stocking of predatory

pikeperch (Sander lucioperca (L.)), although the exact

mechanisms behind their effects remain obscure.

Starting in 2010, oxygen-rich water from the top of

the water column was pumped to the deepest parts of

the lake, resulting in high deepwater oxygen concen-

tration in winter. In summer, hypoxic or even anoxic

conditions could not be avoided, but the duration of

the anoxic period was markedly shortened. Because

nitrate was never depleted, leaching of total nitrogen

from the sediment was reduced and the same was also

true for total phosphorus, but only in winter. The

oxygenation stabilized deepwater nutrient concentra-

tions to a low level, but this was not reflected in the

epilimnetic total nutrient concentration or in a further

decrease in the chlorophyll concentration.

Keywords Biomanipulation � Chlorophyll �Nitrogen � Oxygenation � Phosphorus

Introduction

The recreational and fisheries value of eutrophic lakes

is often damaged by an excessive abundance of

phytoplankton. To alleviate the problems, a large

variety of physical, chemical and biological methods

have been applied in widely different environments.

Specific local conditions and available financing

determine what method, or combination of methods,

and time span of the measures are possible in practice.

A reduction in external loading is the basic method to

Guest editors: Tom Jilbert, Raoul-Marie Couture,

Brian J. Huser & Kalevi Salonen / Restoration of eutrophic

lakes: current practices and future challenges

K. Salonen (&)

Lammi Biological Station, University of Helsinki,

Paajarventie 320, 16900 Lammi, Finland

e-mail: kalevi.salonen@helsinki.fi

J. Sarvala

Department of Biology, University of Turku,

20014 Turku, Finland

J. Horppila � T. Malinen � J. Niemisto

Ecosystems and Environment Research Programme,

University of Helsinki, PO Box 65, 00014 Helsinki,

Finland

J. Keto � I. Malin

Lahti Environmental Services, 15100 Lahti, Finland

J. Ruuhijarvi

Natural Resources Institute Finland, 00791 Helsinki,

Finland

123

Hydrobiologia

https://doi.org/10.1007/s10750-020-04338-3(0123456789().,-volV)( 0123456789().,-volV)

combat eutrophication, but the recovery may involve

considerable delays. To speed up the process, various

in-lake methods have been used. The mainstream

methods may be classified into physical methods,

which target improvement of deepwater oxygen

conditions, chemical, which target a reduction in the

availability of nutrients in water, and biological, which

target shifting the primary control of phytoplankton

from bottom-up to top-down.

Oxygenation of deep lake water has been widely

used in restoration projects all over the world (Beutel

& Horne, 1999; Bormans et al., 2016). It is based on

the theory that when the surface sediment becomes

anoxic, ferric iron is reduced to ferrous iron, which

releases the bound phosphate (Einsele, 1936; Mor-

timer, 1941). Consequently, oxygen depletion leads to

increased nutrient concentrations, which enhance

primary production with its associated problems in

water quality. However, the opposite conclusion, that

anoxia is the consequence rather than the cause of

elevated nutrient concentrations (Gachter & Wehrli,

1998; Hupfer & Lewandowski, 2008; Salmi et al.,

2014), has increasingly resonated with scientists.

Indeed, the ferric iron—phosphorus (P) theory has

long been proposed to be an oversimplification (Lee

et al., 1977), but only rather recently have critical

views been taken more seriously (Nygren et al., 2017).

With full lift aeration or pumping of epilimnetic water

into the hypolimnion it is difficult to increase

hypolimnetic oxygen concentrations above 2 g m-3

in late summer (Liboriussen et al., 2009; Salmi et al.,

2014; Kuha et al., 2016) and water temperature is

increased (Beutel & Horne, 1999; Bryant et al., 2011;

Salmi et al., 2014), accelerating hypolimnetic decom-

position. The use of pure oxygen instead of air

provides much higher oxygenation efficiency (Beutel

& Horne, 1999), but its running costs are high.

Biomanipulation by fish removal has also been

widely used in attempts to limit problems following

phytoplankton blooms. The basic idea is simple and

repeatedly validated experimentally: when predation

on grazers is low, zooplankton are able to control

phytoplankton biomass so that water quality is

improved. Similar to oxygenation, biomanipulation

has often been taken as too simple and the results have

been mixed (Hansson et al., 1998; Drenner & Ham-

bright, 2002; Mehner, 2010; Bernes et al., 2015). The

interpretation of the results is prone to many kinds of

pitfalls, which makes conclusions challenging. In

particular, the time span of studies is often too short so

that all effects may not have had time to be realized.

Various measures are also typically taken simultane-

ously, making it impossible to differentiate between

their individual effects. Moreover, as pointed out by

Horppila et al. (1998), when many indirect effects with

various time spans are coupled with stochastic vari-

ation in weather, the outcome often becomes impos-

sible to interpret. Finally, because the failures of the

measures likely have been under-reported in the

literature and research reports may overemphasize

positive aspects at the expense of negative ones, the

overall conclusions may also be biased to an unknown

extent.

Multifaceted studies with a long time span improve

possibilities to interpret the results but still the same

problems largely exist, and due to economic reasons,

such approaches are rare. Replication of lake-scale

results is virtually impossible and reference lakes are

often lacking. Consequently, final conclusions can

generally be approached only after the analysis of

many studies covering various methods and different

lake types. The present documentation of the long-

term efforts to improve the water quality of Lake

Vesijarvi adds to the knowledge contributing to the

synthesis of different remediation methods. The

restoration history of Lake Vesijarvi has the advan-

tages of a long time span, a wide variety of measure-

ments and to some extent also the possibility to

scrutinize the effects of the measures against the

results of another basin of the same lake and a

neighbouring lake.

Study lake and methods

Lake Vesijarvi (Fig. 1), in southern Finland, is a

seepage lake located between the Salpausselka ridges

to the north and south. Its Enonselka basin, which

formerly received the waste water of the city of Lahti,

is characterized by a rather long retention time of

5.6 years. Water from the Enonselka basin flows to the

Kajaanselka basin, whose residence time is less than

half that of the Enonselka basin (Table 1).

The water quality of Lake Vesijarvi deteriorated

mainly due to municipal waste water of the nearby city

of Lahti. In the 1970s, sewage water of 60,000

inhabitants was discharged almost untreated into the

Enonselka basin, which led to a loss of its value for

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Hydrobiologia

local citizens. The first step in the improvement of the

water quality of the lake was taken when a waste-water

treatment plant was taken into service and its effluent

led away from the catchment area of Lake Vesijarvi. In

1975, the effluent load was cut to a third and additional

cuts in the following year decreased the original

external load of roughly 2 g m-2 P year-1 to Lake

Vesijarvi by an order of magnitude (Keto & Sam-

malkorpi, 1988). In the 1980s, the diversion of

industrial waste water further reduced the nutrient

load by * 15% (Horppila et al., 1998). In spite of the

radical decrease in external load, after less than

10 years the Enonselka basin was plagued by mass

blooms of cyanobacteria throughout the year, which

led to attempts to reinforce the recovery of the basin by

various methods, as outlined by Keto & Sammalkorpi

(1988). Many approaches were tested at different

scales, but the main ones were a further reduction in

the external load, oxygenation of the hypolimnion, as

well as biomanipulation by removal of planktivorous

and benthivorous fish and stocking of predatory fish.

The results until the mid-2000s have been summarized

by Keto et al. (2005) and the later deepwater

oxygenation period by Salmi et al. (2014).

To increase oxygen concentration in deep water, in

1979–1984, a pump station was installed at the deepest

part of the Enonselka basin and it was operated in

winter. In 1983, the number of pumps was increased to

three and they were operated also in summer. Water

was pumped from 1 m depth to the hypolimnion

8–10 m above the sediment to avoid resuspension. For

simplicity in the following, the term ‘oxygenation’ is

Fig. 1 a The main basins of Lake Vesijarvi with its catchment area and sampling points (circles) and b bathymetric map of the

Enonselka basin with the locations of the oxygenation stations (dots). Yellow—fields; green—forests

Table 1 Basic characteristics of Lake Vesijarvi and its study basins (Kuusisto, 2012)

Enonselka Kajaanselka Whole lake

Area (km2) 32a 44 109

Catchment area (km2) 181a 138 514

Maximum depth (m) 33 42 42

Mean depth (m) 6.8 6.8 6.0

Residence time (years) 5.6a 2.4 6.8

aIncluding Paimelanlahti and its associated Vahaselka basin

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Hydrobiologia

used to describe the introduction of oxic epilimnetic

water into the hypolimnion. From 2010, the same

approach (Lappalainen, 1994; Bendtsen et al., 2013)

was applied at a large scale with eight 2.5 kW pump

stations and one 1.5 kW station located above the deep

water of the Enonselka basin (Fig. 1b). To save

energy, in some winters only part of the pumps were

operated (Table 2). The detailed operation times of the

pumps in summer are given by Ruuhijarvi et al.

(2020).

The mass removal of planktivorous and benthivo-

rous fish from the Enonselka basin was performed in

May–August (Keto & Tallberg, 2000) by trawling

over the areas deeper than 10 m (in 1989) or 5–6 m (in

1990–1993). From 1994, trawling was replaced by

fyke net fishing in spring–summer and seine fishing in

autumn. Weather data were obtained from the Lahti

Laune weather station of the Finnish Meteorological

Institute. Chemical and physical determinations were

made in the laboratories of local and regional author-

ities using standard methods similar to those described

by Horppila et al. (1998). Most results are available

from the service of the Finnish Environment Institute

(27 February 2020, https://www.syke.fi/en-US/Open_

information/Open_web_services). Some total P (TP)

and total nitrogen (TN) results were taken from Keto

(1982). Special attention was paid to the results of late

summer, because it is then that water quality problems

are typically emphasized.

The graphics as well as the correlation and regres-

sion statistics calculations of the results were made

with Microsoft Excel 2016. Theoretical dilution

curves of waste water since its diversion were

estimated from the initial and final concentrations of

the time series and from the 5.6-year residence time (r)

according to the formula

y ¼ c0� ctð Þ � 1 � 1=rð Þnþ ct

where y = concentration n years after the sewage

diversion, c0 = initial concentration and ct = final

concentration (estimated from the mean of the last

15 years corrected for the dilution during that time).

From 1988, atmospheric deposition of inorganic N

was measured by the Finnish Meteorological Institute

within a pristine forest area at a distance of * 40 km

from Lake Vesijarvi. Atmospheric deposition of P on

the lake surface was estimated at two stations near the

shore of Lake Vesijarvi in 2008–2009 (Autio & Malin,

unpublished report). The statistics of fertilizers used in

agriculture were compiled by the Natural Resources

Institute Finland (27 February 2020, http://statdb.luke.

fi/PXWeb/pxweb/fi/LUKE/LUKE__08%20Indikaatto

rit__06%20Ymparisto__12%20Typpi-%20ja%20fosf

oritase/02_Kasviravinteiden_myynti.px/?rxid=e11910

8e-bd95-43bf-b02c-a5f4ff9eef72).

Results

In June–August 1975–2018, air temperature (Fig. 2)

increased on average by 2.1�C (SD 0.9�C, where SD is

standard deviation of the mean). However, during the

most intensive fish removal period (Fig. 3), mean

summer temperature consistently decreased by

Table 2 Number of

operative pump stations in

the study years

Year Winter Summer

2009 0 0

2010 8 8

2011 4 7

2012 8 8

2013 8 8

2014 8 7 (6)

2015 3 9

2016 9 8

2017 3 7

2018 4 0

13

15

17

19

21

0

200

400

600

800

1000

1975

1980

1985

1990

1995

2000

2005

2010

2015

2020

Tem

pera

ture

(o C)

Prec

ipita

tion

(mm

year

-1)

Fig. 2 Annual precipitation (dotted lines) and mean air

temperature (solid line with a trend line) in June–August.

Shaded area—intensive fish removal period

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Hydrobiologia

* 2.5�C. Annual precipitation did not change signif-

icantly, but there were different phases. From 1977 to

1985, the interannual variation was high, while during

the following 13 years there was a rather smooth *160 mm decrease (SD 36 mm year-1 after the

removal of the variation explained by linear regression

for that period). After 1998, the interannual variation

(SD 103 mm year-1) returned to the level prevailing

at the beginning of the study.

After the diversion of waste water, some other

components of external nutrient load to Lake Vesijarvi

also decreased. Coincident with the intensive fish

removal, after 1988 N deposition halved within

10 years (Fig. 4), but later its decrease was slower.

Atmospheric deposition of P on the lake surface in

2008–2009 (Autio & Malin, unpublished report) was

0.02 g P m-2 year-1. If the same decrease as observed

for N is applied for P, then it would mean that

atmospheric deposition was about 4% of the total load

of P to the Enonselka basin in 2008–2009, corre-

sponding to about 12% by 1988. Between 1988 and

1997, the amount of P fertilizer used in agriculture in

Finland decreased by 63% and after that 18% more,

while the respective decreases of N fertilizer were

12% and 14%.

Temperature and oxygen in deep water

Before the installation of the pump stations in the

Enonselka basin to oxygenate the hypolimnion, the

maximum temperature at 29 m depth before the

autumnal overturn varied between 9 and 15�C without

any significant trend. Oxygen concentration was

always\ 1.5 g m-3 and often depleted (concentra-

tion before oxygenation\ 0.4 g m-3 in 25 of 33

cases) at the end of the summer stratification (Fig. 5).

The longest period of consistent anoxia at 29 m in

summer occurred in the mid-2000s. Due to variable

weather conditions, sometimes significant deepening

of the thermocline was observed already before the

sampling in August and then the results of July were

used to approximate the distance between the surface

and the depth where hypoxic conditions started

(Fig. 6). Following the decreasing trend in mean

summer temperature during the intensive fish removal

(Fig. 2), the depth of 2 g m-3 oxygen concentration

shifted from 10–15 m depth to about 20 m. In

1997–2009, the stratification of oxygen was again

similar to that before 1986. Because water temperature

explained little (1977–2009 R2\ 0.01 in late summer)

of the variation in deepwater oxygen concentration,

wind episodes in early summer must have played a

dominant role in the variation of hypolimnetic oxygen

conditions. In the Kajaanselka basin, oxygen concen-

tration at 36–40 m depth was never depleted. Its

increasing concentration from the end of the1980s

(Fig. 6) was consistent with the decreasing thickness

0

20

40

60

80

100

1975

1980

1985

1990

1995

2000

2005

2010

2015

2020

Fish

rem

oval

(kg

ha-1

year

-1)

Enonselkä

Kajaanselkä

Fig. 3 Catches of planktivorous and benthivorous fish from the

Enonselka and Kajaanselka basins1986–2018

0

0.2

0.4

0.6

0.8

0

20

40

60

80

100

120

1975

1980

1985

1990

1995

2000

2005

2010

2015

2020

N d

epos

ition

(g m

-2ye

ar-1

)

Fert

ilize

rs(k

g ha

-1)

PhosphorusNitrogenN deposition

Fig. 4 Amount of fertilizers sold to farmers in Finland and

atmospheric deposition of inorganic nitrogen

123

Hydrobiologia

of the hypoxic hypolimnion in the Enonselka basin

(Fig. 5), corroborating enhancement of mixing by

weather conditions in both basins. The oxygenation

increased the upper range of deepwater temperature in

the Enonselka basin to 18�C (Fig. 7), but despite the

generally increasing oxygen concentration, the hypo-

limnion remained hypoxic or sometimes even anoxic

in late summer.

In winter, the temperature at 29 m in the Enonselka

basin varied between 2.8 and 4.5�C before the

oxygenation, which partly explains the higher oxygen

concentration and less frequent anoxia than in sum-

mer. Temperatures sometimes exceeding the maxi-

mum density temperature of water near the bottom

indicated chemical stratification, which is an impor-

tant factor potentially delaying and shortening the

spring overturn. Oxygenation of the Enonselka basin

after 2009 decreased the deepwater winter tempera-

ture by * 2�C and increased oxygen concentration to

7.6–11.3 g m-3. Even the less powerful pump located

at the sampling station in the early 1980s

achieved * 7 g m-3 oxygen concentration in the

0

2

4

6

8

10

12

1975

1980

1985

1990

1995

2000

2005

2010

2015

2020

Oxy

gen

(g m

-3)

0

2

4

6

8

10

12

1975

1980

1985

1990

1995

2000

2005

2010

2015

2020

Oxy

gen

(g m

-3)

KajaanselkäEnonselkä

a bFig. 5 Oxygen

concentration in deep water

of the Enonselka (29 m,

black lines) and Kajaanselka

basins (36–40 m, shaded

area) basins a before the

autumnal overturn and b in

winter

0

5

10

15

20

25

30

Dept

h (m

)

0

5

10

15

20

25

30

Dept

h (m

)

1975 1980 1985 1990 1995

2000 2005 2010 2015

Fig. 6 Vertical distribution

of oxygen concentration in

July–August of 1975–2018

before the beginning of

autumnal deepening of the

epilimnion. Each

distribution is shifted by

5 g m-3 to the right; the

oxygen scale is in 5 g m-3

steps and the years are

shown at zero concentration;

black lines with dots

represent the depth of the

2 g m-3 concentration.

Thick red dashed lines

indicate the intensive fish

removal (upper panel) and

oxygenation periods (lower

panel)

123

Hydrobiologia

deep water. In the Kajaanselka basin, deepwater

oxygen concentration was also generally hypoxic,

but in spite of the greater depth it was never depleted.

Development of nutrient concentrations

in the uppermost water layers

In May–June, TP and TN concentrations at 1 m depth

in the Enonselka basin decreased more or less in

parallel after the diversion of waste water (Fig. 8a, b).

In July–August, the concentration of TP was consis-

tently higher than in May–June, but the difference

narrowed from 1.6 times at the beginning of the study

period to 1.2 times in 2018. Instead, there was no

significant difference in the TN concentration between

early and late summer (Sign test z = 0, P[ 0.10,

P = probability). The decreases in TP and TN con-

centrations were roughly explained by the dilution

model (R2 = 0.69 and 0.39 in May–June and 0.64 and

0.59 in July–August, respectively, R2 = coefficient of

determination). In July–August, both TP and TN

developed initially as predicted by the model, but in

the mid-1980s, when exceptionally high pH values of

up to 9.5 were measured (Fig. 8f), a positive anomaly

in relation to the dilution curve developed. The

concentrations of TP and TN started to decrease after

1987 with a particularly marked step downward

between 1992 and 1993. The concentrations of both

nutrients after the late 1990s roughly followed the

dilution curve and made a single cluster without any

temporal trend (Fig. 9a), indicating that a rather

stable state had been reached. The final concentrations

were about 0.03 g m-3 for TP and 0.45 g m-3 for TN.

The TN:TP mass ratio remained rather similar

throughout the study period. No correlation was found

between TP and the depth where oxygen concentration

reached 2 g m-3. With the exception of TP in the late

1970s, the concentrations of TP and TN in the

Kajaanselka basin were similar in early and late

summer (Fig. 8a). The results in the Enonselka basin

were an average 2.2 (SD = 0.5) and 1.4 (SD = 0.2)

times, respectively, higher than those of the Kajaan-

selka basin. In the time series of the Kajaanselka basin,

there was no sign of the sudden decrease in concen-

tration between 1992 and 1993 found in the Enonselka

basin, but the relationship between the TP values in

both basins stabilized after about 1993 (Fig. 8e).

Compared with the years 2001–2009, the oxygenation

during 2010–2018 did not cause a significant differ-

ence (Mann–Whitney U test) in TP and TN concen-

tration of the Enonselka basin.

In March to early April, total nutrient concentra-

tions at 1 m depth in the Enonselka basin were

occasionally very high between 1984 and 1989

(Fig. 10), and the same happened once in the

Kajaanselka basin. The high concentrations at the

depth nearest to the surface at the same time suggest

that they were due to meltwaters, which depend on the

timing of the late winter sampling. Because of these

irregularities, the data from 15 m depth in the

Enonselka basin were used to fit the dilution curve.

However, although the concentrations at 15 m depth

were slightly higher, the overall development of the

nutrient concentrations at 1 m and 15 m depths during

winter was similar. The dilution model explained most

of the variation (R2 = 0.87) of TP at 15 m depth, but

the respective value for TN (R2 = 0.50) was slightly

lower than in summer. At the end of the study, the

concentrations of TP and TN in the Enonselka basin

were about 1.4 times higher than those in the

Kajaanselka basin.

Other long time series of the lakes in the vicinity of

Lake Vesijarvi were available only from more olig-

otrophic Lake Paajarvi (area 13 km2, depth 85 m),

which is located 6 km west of Lake Vesijarvi. The

land use of its catchment area is comparable with Lake

Vesijarvi: forests 57% (Lake Vesijarvi 60%) and

agricultural fields 18% (23%). Between 1981 and

Fig. 7 Water temperature at 29 m depth of the Enonselka basin

in August (solid line) and March to early April (dashed line).

The maximum density temperature of water is marked by a

dotted line

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Hydrobiologia

2018, epilimnetic TP concentration of Lake Paajarvi

decreased (Fig. 11) by roughly 25% (R2 = 0.21,

P = 0.02), while the respective decrease in the

Kajaanselka basin was roughly 30%. Thus, in addition

to possible regional improvement, decreased TP

concentration of the Kajaanselka basin probably also

reflected decreased nutrient inflow from the Enonselka

basin.

Development of nutrient concentrations in deep

water

In July–August, the deepwater concentrations of TP

and TN in the Enonselka basin were an order of

magnitude higher than in the epilimnion (Fig. 12a, b),

but between 1977 and 2009 their rates of decrease

were faster, roughly 95% vs 40% in TP and 75% vs

50% in TN. Following the most rapid recovery,

between 1998 and 2009 the concentrations of TP and

TN were on average 4.7 and 2.6 times higher,

respectively, than in the Kajaanselka basin.

Coefficient of variation (CV) was much higher in the

Enonselka than Kajaanselka basin, 67% of the mean vs

18% for TP and 22% vs 8% for TN. In March–April,

the concentrations of TP and TN only very weakly

followed the dilution trend. Instead, they showed

irregular alternation between a rather stable low level,

typically slightly lower than in summer, and up to an

order of magnitude higher concentrations (Fig. 12c,

d), which occurred in the years when oxygen concen-

tration decreased below 2 g m-3. It was notable that

low and high concentrations often occurred in succes-

sive years. The burst of nutrients from the sediment

was particularly striking in 1986 and this event also

extended over several years. In the Kajaanselka basin,

TP and TN concentrations closely corresponded to the

lowest levels of the Enonselka basin. The high

difference in TP and TN concentrations between the

basins in July–August despite a negligible difference

in March–April probably reflected higher primary

production and sedimentation of phytoplankton in the

Enonselka basin. The only detailed vertical series of

0

0.02

0.04

0.06

0.08

1975

1980

1985

1990

1995

2000

2005

2010

2015

2020

Tota

l P (g

m-3

)

0

1

2

3

4

1975

1980

1985

1990

1995

2000

2005

2010

2015

2020

1975

1980

1985

1990

1995

2000

2005

2010

2015

2020

Secc

hi d

epth

(m)

6

7

8

9

pH

e

f

49.5

Total phosphorus

Secchi depth

0

0.2

0.4

0.6

0.8

1

1975

1980

1985

1990

1995

2000

2005

2010

2015

2020

Tota

l N (g

m-3

)

0

10

20

30

40

1975

1980

1985

1990

1995

2000

2005

2010

2015

2020

Chlo

roph

yll a

(mg

m- 3

)

0

1

2

3

4

1

2

3

4

1975

1980

1985

1990

1995

2000

2005

2010

2015

2020

TP (E

nons

elkä

/Kaj

aans

elkä

)

Secc

hi d

epth

(Kaj

aans

elkä

/Eno

nsel

kä)

a c

b d

Fig. 8 a Three-year moving averages of total phosphorus,

b total nitrogen, c chlorophyll a and d Secchi depth of the

Enonselka (black lines) and Kajaanselka (orange lines) basins in

May–June (thin lines) and July–August (bold lines); e compar-

ison of the results of the Enonselka and Kajaanselka basins for

mean concentration of TP (blue lines) and Secchi depth (green

lines) in July–August (thick lines) with their superimposed

counterparts in May–June (thin lines); f variation in pH of the

Enonselka basin at 1 m depth in summer. Dotted lines—

development of concentration in the Enonselka basin fitted to

the dilution model; shaded vertical bars—intensive fish removal

period; circles—mean values in July–August

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Hydrobiologia

b d

0.2

2.0

0.02 0.20 2.00

Tota

l N (g

m-3

)

Total P (g m-3)

EnonselkäJuly-August 29 m

77

7983

85

78

8684

80

82

81

87

88

0.2

2.0

0.02 0.20 2.00

Tota

l N (g

m-3

)

Total P (g m-3)

EnonselkäMarch-April 29 m

86

78

87

88

8580

8284 83

0.3

3.0

0.01 0.10

Tota

l N (g

m-3

)

Enonselkä July-August 1 m

1977-19881994-19971998-20092010-20181989-1993

91

90

0.3

3.0

0.01 0.10

Tota

l N (g

m-3

)

KajaanselkäJuly-August 1 m

92

0.3

3.0

0.01 0.10

Tota

l N (g

m-3

)

Enonselkä March-April 1 m

93

a c e

Fig. 9 Relationship between total phosphorus and total nitro-

gen in the Enonselka and Kajaanselka basins in 1977–2018.

Dashed line—Redfield N:P mass ratio of 7:1; upper dotted

line—20:1; lower dotted line—3:1; the time series of the period

1977–1988 is shown by solid lines and numbers denote the last

two digits of the sampling years

0

0.02

0.04

0.06

0.08

1975

1980

1985

1990

1995

2000

2005

2010

2015

2020

Tota

l P (g

m-3

)

0

0.5

1

1.5

219

75

1980

1985

1990

1995

2000

2005

2010

2015

2020

Tota

l N (g

m-3

)

Enonselkä 1 mEnonselkä 15 mKajaanselkä 1 mKajaanselkä 5 m

Fig. 10 Concentrations of

total phosphorus and total

nitrogen at 1 m and 15 m

depths of the Enonselka

basin and at 1 m and 5 m

depths of the Kajaanselka

basin in March–April.

Dotted curve—dilution

model of the Enonselka

basin (15 m)

5

10

15

20

Chlo

roph

ylla

(mg

m-3

)

R² = 0.21

0

0.005

0.01

0.015

0.02

1980

1985

1990

1995

2000

2005

2010

2015

2020

0

1980

1985

1990

1995

2000

2005

2010

2015

2020

Tota

l P (g

m-3

)

a bFig. 11 a Annual mean

concentration of total

phosphorus (in August) and

b all summer observations

of chlorophyll a in Lake

Paajarvi

123

Hydrobiologia

samples from the winter of 1990 showed an extremely

steep gradient of 1.6 g m-3 in TP within a 1.7 m depth

interval near the sediment. Consequently, on the basis

of these results and bathymetric data of the Enonselka

basin, TP in water deeper than 15 m con-

tributed * 6% to the TP concentration of the whole

water mass of the Enonselka basin. The oxygenation

stabilized deepwater TP concentration of the Enon-

selka basin in summer to a level corresponding to the

lowest earlier results, but the average TN concentra-

tion was roughly halved.

The relationship between oxygen and the main

nutrients in deep water was close to hyperbolic

particularly in winter. When oxygen decreased below

2 g m-3, low as well as high nutrient concentrations

were found both in summer and in winter, but

concentrations were always low at higher oxygen

levels. The respective relationship to nitrate was even

more strongly hyperbolic (Fig. 13), showing that after

the depletion of oxygen, P release from the sediment

was accelerated only if nitrate was also exhausted.

The development of the TN:TP ratio was more

dynamic in the deep water than in the upper layers

(Fig. 9). At the beginning of the recovery of the

Enonselka basin, the TN:TP mass ratio was less than 3

in winter, well below the Redfield ratio, indicating N

deficiency, but along with the decrease in total

nutrients in the early 1980s it shifted to higher than

the Redfield ratio, indicating P deficiency of phyto-

plankton. However, at the time of the increased

nutrient release from the sediment in 1986 (Fig. 9),

the TN:TP ratio returned to about 3. During the

intensive fish removal, a shift back towards the ratio

prevailing in 1981–1984 occurred. Although the

TN:TP ratio finally stabilized at about 20, in the years

1996, 2003 and 2009 with temporarily increased

nutrient concentrations, lower TN:TP ratios were

again observed. In late summer, TP and TN concen-

trations (with r = 0.80) as well as their ratio developed

similarly, but the changes were smaller and the

variation was higher than in winter. In winter, the

oxygenation did not affect the TN:TP ratio, but in

summer it shifted close to the Redfield ratio. Shutting

down the pump stations for the summer of 2018

increased the respective TN:TP ratio again to about

20.

5.4 2.0

0

2

4

6

1975

1980

1985

1990

1995

2000

2005

2010

2015

2020

Tota

l N (g

m-3

)0

0.5

1

1.5

1975

1980

1985

1990

1995

2000

2005

2010

2015

2020

Tota

l P (g

m-3

)

0

0.5

1

1.5

1975

1980

1985

1990

1995

2000

2005

2010

2015

2020

Tota

l P (g

m-3

)

Kajaanselkä

Enonselkä

0

2

4

6

1975

1980

1985

1990

1995

2000

2005

2010

2015

2020

Tota

l N (g

m-3

)

a c

b d

Fig. 12 Concentration of

total phosphorus and total

nitrogen in deep water of the

Enonselka (29 m) and

Kajaanselka (39 m) basins

in August (a–b) and in

March–April (c–d)

123

Hydrobiologia

Chlorophyll a

The chlorophyll concentration of the Enonselka basin

was higher in late than in early summer, but after the

intensive fish removal the difference disappeared

(Fig. 8c). The dilution model poorly described the

chlorophyll results in July–August, but its application

pointed to interesting anomalies in relation to the

biomanipulation. The concentrations of TP and TN as

well as chlorophyll began to decrease after the

diversion of sewage (Fig. 8a–c), but almost 10 years

later the favourable development was interrupted and

the concentration remained around 30 mg m-3 until

the end of 1988. During the intensive fish removal

years and 4 years following, the concentration of

chlorophyll decreased about 85% and reached about a

30% lower level than predicted by the dilution curve.

At the same time, its variation in relation to its

respective trend line was much lower than before.

After 1997, the concentration of chlorophyll started to

increase and was an average of * 20% of that at the

time of waste-water diversion. The oxygenation had

no detectable effect on chlorophyll concentration.

The overall trend in chlorophyll concentration in

the Kajaanselka basin (Fig. 8c) was similar to that in

the Enonselka basin in July–August (R2 = 0.46,

P\ 0.001) but at a * 50% lower level, which closely

corresponded to the respective relationship in epilim-

netic TP concentration. The chlorophyll concentration

of the Enonselka basin was nearest to that in the

Kajaanselka basin soon after the fish removal, sug-

gesting that its effect was delayed. The decrease in

chlorophyll concentration as well as the trend in the

chlorophyll:TP ratio in the Kajaanselka basin were not

statistically significant. However, the chlorophyll:TP

ratio in the Kajaanselka basin correlated significantly

with that in the Enonselka basin (r = 0.52, P\ 0.01).

Because the fish removal of the Kajaanselka basin

started only in 1997 and catches were small (Fig. 3),

these hardly affected its water quality. In nearby Lake

Paajarvi, no significant trend was found in chlorophyll

or the chlorophyll:TP ratio from 1980 (Fig. 11).

Before the end of the intensive fish removal, the

ratio between chlorophyll and the TP concentration of

the Enonselka basin in July–August (Fig. 14) mostly

indicated the dominance of small herbivorous zoo-

plankton (Mazumder, 1994), but later until the early

2000s there was a marked shift towards values

indicating the dominance of large herbivores, sug-

gesting an improvement in water quality. In the 2000s,

the variation in the chlorophyll:TP ratio markedly

increased, remaining high throughout the oxygenation

years. The mean chlorophyll:TP ratio between 1998

and 2009 was not significantly different from that

between 2010 and 2018 (Mann–Whitney U test,

P = 0.32), indicating a negligible effect of oxygena-

tion. While the chlorophyll:TP ratio of the Enonselka

basin only temporarily indicated the dominance of

large zooplankton, in the Kajaanselka basin the change

was permanent.

0

0.5

1

1.5

2

0 0.2 0.4

Tota

l P (g

m-3

)

Nitrate N (g m-3)

Winter 1977-2009

Winter 2010-2018

Summer 1977-2009

Summer 2010-2018

0

1

2

3

4

5

6

0 0.2 0.4

Tota

l N (g

m- 3

)

Nitrate N (g m-3)

Fig. 13 Relationship of total phosphorus and total nitrogen to nitrate concentration at 29 m depth in the Enonselka basin. The arrows

show the shift in the year when the pump stations were stopped for summer

123

Hydrobiologia

Secchi depth

During the fish removal, the Secchi depth of the

Enonselka basin increased significantly (Mann–Whit-

ney U test, P\ 0.01) from about 1.5 m to 2.5–3 m in

1994–1997. Between 1988 and 1998, the variation

between successive years was remarkably low and at

the end of this period the values were at their lowest in

relation to the Kajaanselka basin (Fig. 8e). Similar to

chlorophyll during the last 15 years, the variation in

the Secchi depth of the Enonselka basin was high. In

the Kajaanselka basin, the Secchi depth was on

average 1.4 m higher than that in the Enonselka basin

both in early and late summer and their time courses

were quite similar (Fig. 8d).

Discussion

The dilution of waste water formerly discharged into

the Enonselka basin was the main reason for its

recovery. This conclusion was strongly supported by

the high agreement between the observed total nutrient

concentrations and those of the respective dilution

curves in winter (Fig. 10), when conditions under the

ice are undisturbed by weather, primary producers and

inflow, and thermal as well as chemical stratification

separate the shallow and deepwater layers from each

other (Salmi et al., 2014). Although the dilution of

nutrients varied interannually depending on the vari-

ation in hydrology, internal loading (Søndergaard

et al., 1993; Jilbert et al., this issue), atmospheric

deposition and the use of fertilizers in agriculture

(Fig. 4), the simple application of the average resi-

dence time to calculate the dilution provided a useful

background for the interpretation of the results.

Because agriculture is responsible for * 40% of the

total P load to the Enonselka basin, its * 80%

decrease between 1988 and 1997 means a dramatic

change in potential nutrient resources for phytoplank-

ton. However, because P is tightly bound to the soil, its

leaching is strongly delayed (Carpenter, 2005).

Accordingly, the P load from the most important

inflowing streams and brooks as well as from urban

run-off to Lake Vesijarvi (unpublished results of Lahti

Environmental Services) decreased only * 14%

between 1987 and 2015.

The oxygenation of the Enonselka basin in summer

delayed the depletion of hypolimnetic oxygen, but it

also decreased the temperature gradient between the

epi- and hypolimnion, which advanced the beginning

of the autumnal overturn. Consequently, the time was

too short to deplete nitrate (Fig. 13) and redox

potential remained high enough to keep P in the

sediment (Andersen, 1982). On the other hand, the

intensified coupling of nitrification and denitrification

in deep water due to the oxygenation (Beutel, 2006;

Salmi et al., 2014; Holmroos et al., 2016) was

evidently responsible for the decreased TN concen-

tration (Fig. 12b, d). In spite of the reduced leaching of

both TP and TN from the deepwater sediment, the

effect of the oxygenation in the epilimnion remained

1

10

100

0.01 0.10

Chlo

roph

yll a

(mg

m-3

)

Total phosphorus (mg m-3)

19972001

2010

19962000

20092018 1983

19822013

1989

Enonselkä Kajaanselkä

1

10

100

0.01 0.10

Chlo

roph

yll a

(mg

m-3

)

Total phosphorus (mg m-3)

1979-1988Intensive fish removal1994-19971998-2009Oxygenation

19972009

2010

2001

1980

1979

2016

20042003

19821983

19891988

1985

Fig. 14 Interannual variation in the relationship between mean

chlorophyll and total phosphorus in the Enonselka and

Kajaanselka basins in July–August. The regression lines

suggested by Mazumder (1994) indicating the dominance of

large (dotted line) and small (solid line) zooplankton are shown

for comparison. Thick lines show the time sequence of the years

between 1989 and 1997

123

Hydrobiologia

undetectable as also found elsewhere (Liboriussen

et al., 2009; Kuha et al., 2016). Elevated temperature

increased the mineralization of organic matter (Salmi

et al., 2014; Niemisto et al., 2020) and fewer nutrients

were probably buried in the sediment. Originally it

was also hoped that the oxygen consumption of the

sediment would gradually decrease, but in agreement

with Engstrom & Wright (2002) who found no loss of

organic sediment in five lakes aerated/circulated for 8

to 18 years, the results did not support that (Fig. 5).

In their review, Preece et al. (2019) concluded that

oxygenation of the hypolimnion by oxygen gas can be

an important tool ‘when used properly’. Such a

conclusion is certainly valid from the perspective of

deep water and particularly if oxygen gas is applied.

Pumping of epilimnetic water into the hypolimnion is

more economical, but its advantages are limited by

consequent warming of the hypolimnion. The greatly

improved oxygen conditions in deep water and smaller

nutrient leakage from the sediment of the Enonselka

basin after the oxygenation agree with the literature

(Gachter & Wehrli, 1998; Liboriussen et al., 2009).

The absence of a detectable effect on phytoplankton,

an adverse influence on cold water fish and increased

oxygen consumption in the hypolimnion as well as

enhanced recycling of nutrients in the whole water

body (Niemisto et al. 2020) did also not support the

feasibility of the oxygenation. Finally, because the

only extreme burst of nutrients from the sediment

happened 30 years ago and the dilution of the waste

water as well as the decreases in external loading have

been great, precautionary oxygenation is no longer

justified.

A new stable TP level in the Enonselka basin was

reached 10–15 years after the sewage diversion as also

found by Jeppesen et al. (2005) in 35 subtropical and

temperate lakes of various size, depth and trophic

state. Instead, for TN they found stabilization times

of\ 5 years, while in the Enonselka basin the stabi-

lization time was similar to that of TP. This contrast

may arise from the fact that in the Enonselka basin, as

in many other Finnish lakes (e.g. Sarvala et al., this

issue), TN levels reflect dinitrogen fixation, which

closely follows TP concentration. In the data of

Jeppesen et al. (2005), nutrient concentrations are

much higher and this link is weaker.

The internal loading of nutrients released from

anoxic deepwater sediment has been suggested to be

the main P load to many lakes (Nurnberg, 2009), but it

has been questioned in the Enonselka basin (Salmi

et al., 2014). In a study covering a comprehensive set

of lakes, Tammeorg et al. (2017) also demonstrated

that a hypolimnetic oxygen deficit has minor impor-

tance for water quality. However, the longer time

series of the Enonselka basin in the present study

suggests that in the mid-1980s a combination of many

factors led to accelerated internal nutrient loading. Its

prerequisites probably included a short duration of

spring overturn (not measured), decreasing precipita-

tion leading to decreasing nutrient loading (Fig. 2),

and high thickness of the anoxic hypolimnion (Fig. 6).

The latter might have shoaled the metalimnion to so

shallow water that internal seiches (MacIntyre et al.,

1999) strengthened the flux of nutrients from the

anoxic hypolimnion to the epilimnion. Another or

parallel factor may have been the ebullition of gases

(Ohle, 1978), which can abruptly increase the flux of

nutrients from the sediment. Hydroacoustic studies

have indicated a marked decrease in ebullition com-

pared with that in the 1990s (Ruuhijarvi et al., this

issue). The nutrient pulse from the sediment after the

middle of the 1980s probably initiated the develop-

ment of the observed cyanobacteria blooms (Horppila

et al., 1998), which elevated pH to such a level

(Andersen, 1975) that leaching of P from the epilim-

netic sediment increased. In routine samples typically

taken before noon, pH values remained below 9.5,

regarded as critical for P release (Seitzinger, 1991),

but values in late afternoon must have been markedly

higher. Keto & Sammalkorpi (1988) noted a high pH

gradient between the pelagial (9.5–9.7) and the littoral

(10–10.5, sometimes even[ 11) zones. However, due

to typically lower pH in the sediment (Huser et al.,

2016) which has a higher buffer capacity, the desorp-

tion effect of high pH in shallow area sediments may

require resuspension of particles. In addition, Koski-

Vahala et al. (2001) demonstrated that in the Enon-

selka basin the high silicon concentration strongly

increases P concentration in the interstitial water of the

oxic sediment. Interestingly, in 1985 the accumulation

of a small 6–7 lm diameter Stephanodiscus diatom,

often dominant in the Enonselka basin in spring, was

at its highest since the waste-water diversion (Liukko-

nen et al., 1993), which may have amplified the

dissolution of silicon in the sediment. Thus, temporar-

ily increased leaching of P from both the shallow and

deepwater sediment plausibly created a spiral whereby

nutrient leakages from anoxic and oxic sediment were

123

Hydrobiologia

sustaining cyanobacteria blooms and increasing oxy-

gen consumption in the hypolimnion. Hence, although

anoxia in the Enonselka basin has generally been the

consequence rather than the cause of elevated nutrient

concentrations and sediment has been a sink of

nutrients rather than their source, temporary reversals

have been possible under suitable conditions.

The importance of nutrients leaching from the

deepwater sediment is difficult to evaluate, because

the vertical sampling interval is generally too scarce to

cope with the steep concentration gradient in the

neighbourhood of the sediment. In the Enonselka

basin, the depths deeper than 25 m represent only *1% of the total water volume, so that extremely high

concentrations from deep water are needed to cause a

significant increase in the nutrient concentration of the

whole water column. The extrapolation of the detailed

vertical results in winter 1990 to the year 1986, when

TP concentration at 29 m depth was over an order of

magnitude higher, suggests that, exceptionally, nutri-

ent concentrations of the whole water mass can be

substantially elevated. The paradoxical alternation of

low and high concentrations of deepwater nutrients in

winter in different years is another weak point

particularly from the management perspective. The

most likely explanation for the paradox may be the

variation in water and sediment temperatures at the

time of lake freezing. Rather small temperature

differences may create widely contrasting under-ice

flow regimes (Salonen et al., 2014), which can explain

dramatic differences between successive years. If

necessary, consequences unfavourable conditions

could be avoided by oxygenation, but the prediction

of such cases may be challenging.

Development of phytoplankton

Because the Enonselka basin feeds * 20% of the

total inflow into the Kajaanselka basin and its nutrient

concentrations were roughly two times higher in late

summer, it is reasonable that TP, TN and chlorophyll

concentrations as well as Secchi depth in the

Kajaanselka basin roughly followed those of the

Enonselka basin (Fig. 8a–d). The positive anomalies

of nutrient and chlorophyll concentrations in the

respective dilution curves in the late 1980s were

linked to the extremely high internal loading of

nutrients in deep water at the same time in winter

(Fig. 12c, d). However, no respective anomalies were

found in the Kajaanselka basin. The reduced relative

variation in chlorophyll concentration in relation to its

trend line between 1988 and 1997 (Fig. 8c) may have

been due to grazers controlling the development of

high phytoplankton densities in the Enonselka basin.

The low TN:TP ratio in deep water (Fig. 9b, d) in the

last half of the 1980s may have favoured N fixing

cyanobacteria which were dominant in the phyto-

plankton of the following summers. The absence of

phytoplankton responses after respective bursts of

nutrients in later winters can be explained by further

advanced dilution of the waste water, a decreasing

amount of nutrients leaching from the sediment

(Jilbert et al., this issue), a decreasing external loading,

and by a lack of weather-related factors favouring the

internal release of nutrients in successive years.

In agreement with the decrease in phytoplankton

biomass based on microscopic counting (Keto et al.,

2005), about half of the decrease in the concentration

of chlorophyll after its maximum in the late 1980s

happened before the beginning of the intensive fish

removal. Thus, the roughly 90% decrease in the

biomass of cyanobacteria between 1988 and 1990

(Horppila et al., 1998) was likely more due to the

decreasing availability of nutrients than to the bioma-

nipulation. Instead, the decrease of chlorophyll con-

centration that was clearly below the level predicted

by the dilution curve a few years after the intensive fish

removal might be mainly attributed to the biomanip-

ulation. This interpretation is corroborated by the

absence of respective negative anomalies in nutrient

concentrations in relation to their dilution curves

(Fig. 8a, b) as well as the absence of a concomitant

minimum in chlorophyll concentration in the Kajaan-

selka basin around 1997. The ratio between Secchi

depths of both basins (Fig. 8e) also indicates relative

improvement of the Enonselka basin in relation to the

Kajaanselka basin, while that was not the case in the

respective ratio of TP results. No significant change in

the chlorophyll concentration of Lake Paajarvi

between 1988 and 1997 (Fig. 11) suggests no regional

trend that might affect the interpretation of the results

of Lake Vesijarvi. The stabilization of chlorophyll

concentration of the Enonselka basin from 2000

corresponds to the experiences of other lakes in which

a return to a more turbid state typically happens within

10 years or less after biomanipulation (Søndergaard

et al., 2007). The virtual disappearance of the differ-

ence between the chlorophyll concentrations in early

123

Hydrobiologia

and late summer from the early 1990s suggests that the

water quality of the Enonselka basin had permanently

reached a moderate condition in the ecological

classification of the European Union’s Water Frame-

work Directive.

Effect of fish removal

The effects of the 5-year intensive fish removal of the

Enonselka basin were gradually manifested in the

decrease of fishable new recruits of planktivorous and

benthivorous fish. The exceptionally strong year class

of roach in 1988, which appeared from the littoral to

the open water area a few years later (Horppila et al.,

1998), could be removed by trawling. Although fish

are able to move between the basins, the intensive fish

removal predominantly depleted pelagic fish of the

Enonselka basin (Peltonen et al., 1999a, b). Fish

removal meant a 90% decrease in planktivorous roach

and smelt and after the collapse of the roach stock, the

pelagic fish assemblage became smelt dominated with

high year-to-year density variations (Ruuhijarvi et al.,

2005). Similar to experiences elsewhere (e.g. Sarvala

et al. 1998, 2001), the change led to a reduction in

chlorophyll concentration by several parallel and/or

successive mechanisms during and after the bioma-

nipulation. The most direct effect was the removal of

nutrients in fish biomass. According to Boros et al.

(2012) the mean proportion of P in the dry mass of

roach from six European lakes was 2.4%, which quite

closely agrees with the results from four Polish lakes

(Penczak et al., 1985) and Finnish Lake Koylionjarvi

(Tarvainen et al., 2002). This implies (assuming that

dry mass is 25% of wet mass) that in 1989–1993 an

average of 0.007 g P m-2 year-1 was removed from

the Enonselka basin, amounting to roughly 60% of the

respective decrease in the concentration due to

dilution and 12% of the estimated TP load. Thus,

nutrients removed with fish no doubt advanced the

recovery of the Enonselka basin. Removal of nutrients

during a short time at the end of a marked dilution

phase of waste water from the mid-1970s also explains

the stepwise decrease in nutrient concentrations to a

rather stable level in 1993.

The top-down regulation of aquatic food chains

suggested by Shapiro et al. (1975) is a widely accepted

possibility but is influenced by a complex range of

factors including species composition and size distri-

butions of fish, zooplankton and phytoplankton

(Ramcharan et al., 1996), which are further affected

by the plastic behaviour of the organisms as well as

stochastic weather conditions. Attention has often

been placed on the role of large Daphnia species

which are efficient filter feeders able to control

phytoplankton but vulnerable to predation by fish

(Brooks & Dodson, 1965). Because the relative P

content of large Daphnia species is high compared

with other zooplankton (e.g. Hessen & Andersen,

1992), the amount of P bound in their biomass can

have fundamental ecological effects (e.g. Elser et al.,

1996). However, in the Enonselka basin large Daphnia

species have not been prevalent and the increase in

their mean carapace length was\ 5% after the

intensive fish removal (Nykanen et al., 2010). Anttila

et al. (2013) interpreted the decrease in chlorophyll

concentration of the Enonselka basin during the

biomanipulation as a major regime shift which

included two stages, one in 1990 and another in

1993. The results of the present study support only a

change in 1993 (Fig. 9) and even then the evidence

that cladocerans were responsible hardly can be

inferred only from the small increase in the size of

Daphnia. In general, the idea of regime shift is

controversial, because the alleged mechanistic links

between pressures and ecological changes are often

insufficiently demonstrated (Capon et al., 2015). In the

case of the Enonselka basin, the detection of possible

transition points is further hampered by the simulta-

neous dilution of the waste water and the internal

nutrient pulse in the late 1980s as well as the decreases

in atmospheric and fertilizer loadings. Thus, as also

concluded by Horppila et al. (1998), the change in the

phytoplankton was not due to enhanced zooplankton

grazing. There are also other examples that improve-

ments in the water quality of lakes dominated by

planktivorous fish that do not necessarily require

significant changes in cladoceran populations (Ham-

rin, 1993; Sommer et al., 2001; Urrutia-Cordero et al.,

2015) and top-down control of phytoplankton can be

mediated by smaller cladocerans (Helminen & Sar-

vala, 1997).

The effect of the fish removal on phytoplankton of

the Enonselka basin was probably amplified by the

stocking of over a million juvenile pikeperch (Sander

lucioperca (L.)) in 1984–1991, which led to their

reproduction in 1992 and to the establishment of a

strong population supporting fisheries (Kairesalo

et al., 1999). Compared with the 1980s, when open

123

Hydrobiologia

water predatory fish were scarce (Keto & Sammalko-

rpi, 1988), the change was remarkable and in this

respect pikeperch stocking can be regarded as one of

the greatest successes of the biomanipulation of the

Enonselka basin. The restitution of pikeperch seems to

have created a new stable situation where the role of

roach may have permanently declined. As an efficient

open water predator chasing both smelt and roach

(Peltonen et al., 1996), pikeperch probably became a

deterrent keeping roach predominantly out of the

pelagic zone, which was expressed as an increased size

of individuals caught from the open water zone.

Similar behaviour of roach has been found after

pikeperch introduction in Lake Gjersjøen in southern

Norway (Brabrand & Faafeng, 1993). Romare &

Hansson (2003) and Gliwicz (2002) have also shown

that the risk of predation can regulate how roach are

distributed between the littoral and pelagial zones.

Changes in the behaviour of fish and zooplankton

emphasize the importance of sophisticated beha-

vioural adaptations on top of simple mechanistic

trophic relationships and render differentiation and

quantification of various factors involved in bioma-

nipulation extremely challenging.

General discussion

Although the basic mechanisms involved in lake

ecosystems are universal, unique environmental con-

ditions may markedly differ so that caution is needed

particularly when comparing the results of small and

large lakes or shallow and deep ones which have

contrasting hydrodynamics. In lakes, such as Lake

Vesijarvi, which are open to wind, stochastic hydro-

dynamic episodes can modify the food webs with

annual or even longer timescale effects. The ostensible

reversal of the favourable development of the Enon-

selka basin 10 years after the waste-water diversion is

a striking example. Then, as indicated by similar

increases in nutrient and chlorophyll concentrations

between the diversion of the sewage waters and the

end of the 1980s (Fig. 8a–c), the phytoplankton in the

Enonselka basin was largely controlled by bottom-up

factors. Instead, in later years, the low chlorophyll:TP

ratio suggested a shift to the dominance of top-down

factors. The complex interactions of planktivorous and

benthivorous fish as well as macrophytes constitute a

network of direct and indirect linkages between

environmental and biological factors as well as

between organisms at different trophic levels that also

vary with time and space (Kairesalo et al., 1999). In

agreement with Andersson et al. (1988) and Horppila

& Kairesalo (1992) showed experimentally that ben-

thivorous fish may radically increase nutrient flux

from the sediment of the Enonselka basin. Aquatic

macrophytes may also affect phytoplankton by their

nutrient competition (Hansson et al., 1998), but those

were not included in regular monitoring of the

Enonselka basin. Increased water transparency in the

middle of the 1990s allowed macrophytes to expand

their habitat from * 2 m depth to * 4 m depth

(Venetvaara & Lammi, 1995) so that finally they

covered an area with roughly 50% of the water

volume. Because the spreading of macrophytes into a

new habitat and the growth of biomass takes time,

their effects also appear with a delay (Scheffer et al.,

1993). Therefore, the sudden drop in epilimnetic TP

and TN concentrations between 1992 and 1993

(Fig. 9) was most likely mediated by the removal of

benthivorous fish rather than by macrophytes.

Conclusions

The efforts to improve the water quality of the

Enonselka basin of Lake Vesijarvi from 1975 led to

the re-establishment of sustainable fisheries and the

recreational value of the lake. Although the progress

was predominantly due to the diversion of the waste

water and the following dilution, planktivorous and

benthivorous fish removal and the stocking of preda-

tory fish also supported the recovery. The detailed

mechanisms remain unclear, but owing to the long-

term monitoring and diverse approaches including

comparison between the Enonselka and Kajaanselka

basins, the main trend lines of the effects of the

remediation measures could be elicited out of the

multitude of interlinked factors mixed with stochastic

weather conditions. The recovery of the Enonselka

basin has evidently reached a stable phase where the

sediment and external load are the key factors

determining the future recovery trajectory. According

to the present results, the low-level fish removal and

hypolimnetic oxygenation do not have great promise

for the further improvement of water quality.

Acknowledgements Open access funding provided by

University of Helsinki including Helsinki University Central

123

Hydrobiologia

Hospital. This study is a product of the long-term efforts of

many parties. To mention only the main players, the city of Lahti

played a pivotal role in initiating and running the monitoring

programme as well as providing an attractive environment for

various research projects. Numerous persons in many

organizations have contributed to the production of data over

the years. The establishment of the Vesijarvi Foundation greatly

strengthened the Lake Vesijarvi research. We thank the

anonymous reviewers and Tom Jilbert for their constructive

comments. Cathryn Primrose-Mathisen kindly checked the

English language.

Compliance with ethical standards

Conflict of interest The authors declare no conflict of interest.

Open Access This article is licensed under a Creative Com-

mons Attribution 4.0 International License, which permits use,

sharing, adaptation, distribution and reproduction in any med-

ium or format, as long as you give appropriate credit to the

original author(s) and the source, provide a link to the Creative

Commons licence, and indicate if changes were made. The

images or other third party material in this article are included in

the article’s Creative Commons licence, unless indicated

otherwise in a credit line to the material. If material is not

included in the article’s Creative Commons licence and your

intended use is not permitted by statutory regulation or exceeds

the permitted use, you will need to obtain permission directly

from the copyright holder. To view a copy of this licence, visit

http://creativecommons.org/licenses/by/4.0/.

References

Andersen, J. M., 1975. Influence of pH on release of phosphorus

from lake sediments. Archiv fur Hydrobiologie 76:

411–419.

Andersen, J. M., 1982. Effect of nitrate concentration in lake

water on phosphate release from the sediment. Water

Research 16: 1119–1126.

Andersson, G., W. Graneli & J. Stenson, 1988. The influence of

animals on phosphorus cycling in lake ecosystems.

Hydrobiologia 170: 267–284.

Anttila, S., M. Ketola, K. Kuoppamaki & T. Kairesalo, 2013.

Identification of a biomanipulation-driven regime shift in

Lake Vesijarvi: implications for lake management. Fresh-

water Biology 58: 1494–1502.

Bendtsen, J., K. E. Gustafsson, J. Lehtoranta, E. Saarijarvi, K.

Rasmus & H. Pitkanen, 2013. Modeling and tracer release

experiment on forced buoyant plume convection from

coastal oxygenation. Boreal Environment Research 18:

37–52.

Bernes, C., S. R. Carpenter, A. Gardmark, P. Larsson, L. Pers-

son, C. Skov, J. D. M. Speed & E. Van Donk, 2015. What is

the influence of a reduction of planktivorous and benthiv-

orous fish on water quality in temperate eutrophic lakes? A

systematic review. Environmental Evidence 4: 1–28.

Beutel, M. W., 2006. Inhibition of ammonia release from anoxic

profundal sediments in lakes using hypolimnetic oxy-

genation. Ecological Engineering 28: 271–279.

Beutel, M. W. & A. J. Horne, 1999. A review of the effects of

hypolimnetic oxygenation on lake and reservoir water

quality. Lake and Reservoir Management 15: 285–297.

Bormans, M., B. Marsalek & D. Jancula, 2016. Controlling

internal phosphorus loading in lakes by physical methods

to reduce cyanobacterial blooms: a review. Aquatic Ecol-

ogy 50: 407–422.

Boros, G., J. Jyvasjarvi, P. Takacs, A. Mozsar, I. Tatrai, M.

Søndergaard & R. I. Jones, 2012. Between-lake variation in

the elemental composition of roach (Rutilus rutilus L.).

Aquatic Ecology 46: 385–394.

Brabrand, A. & B. Faafeng, 1993. Habitat shift in roach (Rutilus

rutilus) induced by pikeperch (Stizostedion lucioperca)

introduction: predation risk versus pelagic behaviour.

Oecologia 95: 38–46.

Brooks, J. L. & S. I. Dodson, 1965. Predation, body size, and

composition of plankton. Science 150: 28–35.

Bryant, L. D., P. A. Gantzer & J. C. Little, 2011. Increased

sediment oxygen uptake caused by oxygenation-induced

hypolimnetic mixing. Water Research 45: 3692–3703.

Capon, S. J., A. J. J. Lynch, N. Bond, B. C. Chessman, J. Davis,

N. Davidson, M. Finlayson, P. A. Gell, D. Hohnberg, C.

Humphrey, R. T. Kingsford, D. Nielsen, J. R. Thomson, K.

Ward & R. Mac Nally, 2015. Regime shifts, thresholds and

multiple stable states in freshwater ecosystems; a critical

appraisal of the evidence. Science of the Total Environ-

ment 534: 122–130.

Carpenter, S. R., 2005. Eutrophication of aquatic ecosystems:

bistability and soil phosphorus. Proceedings of the

National Academy of Sciences of the United States of

America 102: 1003–1005.

Drenner, R. W. & K. D. Hambright, 2002. Piscivores, trophic

cascades, and lake management. The Scientific World

Journal 2: 284–307.

Einsele, W., 1936. Uber die Beziehungen des Eisenkreislaufs

zum Phosphatkreislauf im eutrophen See. Archiv fur

Hydrobiologie 29: 664–686.

Elser, J. J., D. R. Dobberfuhl, N. A. MacKay & J. H. Schampel,

1996. Organism size, life history, and N: P stoichiometry,

toward a unified view of cellular and ecosystem processes.

BioScience 46: 674–684.

Engstrom, D. R. & D. I. Wright, 2002. Sedimentological effects

of aeration-induced lake circulation. Lake and Reservoir

Management 18: 201–214.

Gliwicz, Z. M., 2002. On the different nature of top-down and

bottom-up effects in pelagic food webs. Freshwater Biol-

ogy 47: 2296–2312.

Gachter, R. & B. Wehrli, 1998. Ten years of artificial mixing

and oxygenation: no effect on the internal phosphorus

loading of two eutrophic lakes. Environmental Science and

Technology 32: 3659–3665.

Hansson, L.-A., H. Annadotter, E. Bergman, S. F. Hamrin, E.

Jeppesen, T. Kairesalo, E. Luokkanen, P.-A. Nilsson, M.

Søndergaard & J. Strand, 1998. Biomanipulation as an

application of food-chain theory: constraints, synthesis,

and recommendations for temperate lakes. Ecosystems 1:

558–574.

Hamrin, S., 1993. Lake restoration by cyprinid control in Satofta

Bay (Lake Ringsjon). Verhandlungen der internationale

Vereinigung fur theoretische und angewandte Limnologie

25: 487–493.

123

Hydrobiologia

Helminen, H. & J. Sarvala, 1997. Responses of Lake Pyhajarvi

(SW Finland) to variable recruitment of the major plank-

tivorous fish, vendace (Coregonus albula). Canadian

Journal of Fisheries and Aquatic Sciences 54: 32–40.

Hessen, D. O. & T. Andersen, 1992. The algae-grazer interface:

feedback mechanisms linked to elemental ratios and

nutrient cycling. Ergebnisse der Limnologie 35: 111–120.

Holmroos, H., J. Horppila, S. Laakso, J. Niemisto & S. Hietanen,

2016. Aeration-induced changes in temperature and

nitrogen dynamics in a dimictic lake. Journal of Environ-

mental Quality 45: 1359–1366.

Horppila, J. & T. Kairesalo, 1992. Impacts of bleak (Alburnus

alburnus) and roach (Rutilus rutilus) on water quality,

sedimentation and internal nutrient loading. Hydrobiologia

243(244): 323–333.

Horppila, J., H. Peltonen, T. Malinen, E. Luokkanen & T.

Kairesalo, 1998. Top-down or bottom-up effects by fish:

issues of concern in biomanipulation of lakes. Restoration

Ecology 6: 20–28.

Hupfer, M. & J. Lewandowski, 2008. Oxygen controls phos-

phorus release from lake sediments – a long lasting para-

digm in limnology. International Review of Hydrobiology

93: 415–432.

Huser, B. J., S. Egemose, H. Harper, M. Hupfer, H. Jensen, K.

M. Pilgrim, K. Reitzel, E. Rydin & M. Futter, 2016.

Longevity and effectiveness of aluminium addition to

reduce sediment phosphorus release and restore lake water

quality. Water Research 97: 122–132.

Jeppesen, E., M. Søndergaard, J. P. Jensen, K. Havens, O.

Anneville, L. Carvalho, M. F. Coveney, R. Deneke, M.

Dokulil, B. Foy, D. Gerdeaux, S. E. Hampton, K. Kangur,

J. Kohler, S. Korner, E. Lammens, T. L. Lauridsen, M.

Manca, R. Miracle, B. Moss, P. Noges, G. Persson, G.

Phillips, R. Portielje, S. Romo, C. L. Schelske, D. Straile, I.

Tatrai, E. Willen & M. Winder, 2005. Lake responses to

reduced nutrient loading – an analysis of contemporary

long-term data from 35 case studies. Freshwater Biology

50: 1747–1771.

Jilbert, T., S. Jokinen, T. Saarinen, U. Mattus-Kumpunen, A.

Simojoki, S. Saarni, S. Salminen, J. Niemisto & J Horppila,

2020. Impacts of a deep reactive layer on sedimentary

phosphorus dynamics in a boreal lake recovering from

eutrophication. Hydrobiologia.

Kairesalo, T., S. Laine, E. Luokkanen, T. Malinen & J. Keto,

1999. Direct and indirect mechanisms behind successful

biomanipulation. Hydrobiologia 395(396): 99–106.

Keto, J., 1982. The recovery of Lake Vesijarvi after sewage

diversion. Hydrobiologia 86: 195–199.

Keto, J. & I. Sammalkorpi, 1988. A fading recovery: a con-

ceptual model for Lake Vesijarvi management and

research. Aqua Fennica 18: 193–204.

Keto, J. & P. Tallberg, 2000. The recovery of Vesijarvi, a lake in

southern Finland: water quality and phytoplankton inter-

pretations. Boreal Environment Research 5: 15–26.

Keto, J., P. Tallberg, I. Malin, P. Vaaranen & K. Vakkilainen,

2005. The horizon of hope for L. Vesijarvi, southern Fin-

land: 30 years of water quality and phytoplankton studies.

Verhandlungen der internationale Vereinigung fur theo-

retische und angewandte Limnologie 29: 448–452.

Koski-Vahala, J., H. Hartikainen & P. Tallberg, 2001. Phos-

phorus mobilization from various sediment pools in

response to increased pH and silicate concentration. Jour-

nal of Environmental Quality 30: 546–552.

Kuha, J. K., A. H. Palomaki, J. T. Keskinen & J. S. Karjalainen,

2016. Negligible effect of hypolimnetic oxygenation on the

trophic state of Lake Jyvasjarvi, Finland. Limnologica 58:

1–6.

Kuusisto E., 2012. Hydrology of Lake Vesijarvi. In: Keto, J., H.

Kolunen, A. Pekkarinen & L. Tuominen (eds), Lake

Vesijarvi daughter of the Salpausselka Ridges: 59–61.

Lappalainen, K. M., 1994. Positive changes in oxygen and

nutrient contents in two Finnish lakes induced by Mixox

hypolimnetic oxygenation method. Verhandlungen der

internationale Vereinigung fur theoretische und ange-

wandte Limnologie 25: 2510–2513.

Lee, G. F., W. C. Sonzogni & R. D. Spear, 1977. Significance of

oxic versus anoxic conditions for lake Mendota sediment

phosphorus release. Proceedings of the International

Symposium on Interactions Between Sediments and Fresh

Water, Amsterdam, W. Junk, The Hague: 294–306.

Liboriussen, L., M. Søndergaard, E. Jeppesen, I. Thorsgaard, S.

Grunfeld, T. S. Jakobsen & K. Hansen, 2009. Effects of

hypolimnetic oxygenation on water quality: results from

five Danish lakes. Hydrobiologia 625: 157–172.

Liukkonen, M., T. Kairesalo & J. Keto, 1993. Eutrophication

and recovery of Lake Vesijarvi (south Finland): Diatom

frustules in varved sediments over a 30-year period.

Hydrobiologia 269(270): 415–426.

Mazumder, A., 1994. Phosphorus-chlorophyll relationships

under contrasting herbivory and thermal stratification:

predictions and patterns. Canadian Journal of Fisheries and

Aquatic Sciences 51: 390–400.

MacIntyre, S., K. M. Flynn, R. Jellison & J. R. Romero, 1999.

Boundary mixing and nutrient flux in Mono Lake, Cali-

fornia. Limnology and Oceanography 44: 512–529.

Mehner, T., 2010. No empirical evidence for community-wide

top-down control of prey fish density and size by fish

predators in lakes. Limnology and Oceanography 55:

203–213.

Mortimer, C. H., 1941. The exchange of dissolved substances

between mud and water in lakes. Journal of Ecology 29:

280–329.

Niemisto, J., S. Silvonen & J. Horppila, 2020. Effects of

hypolimnetic aeration on the quantity and quality of set-

tling material in a eutrophied dimictic lake. Hydrobiologia.

https://doi.org/10.1007/s10750-019-04160-6.

Nurnberg, G. K., 2009. Assessing internal phosphorus load –

problems to be solved. Lake and Reservoir Management

25: 419–432.

Nygren, N. A., P. Tapio & J. Horppila, 2017. Will the oxygen-

phosphorus paradigm persist? – expert views of the future

of management and restoration of eutrophic lakes. Envi-

ronmental Management 60: 947–960.

Nykanen, M., T. Malinen, K. Vakkilainen, M. Liukkonen & T.

Kairesalo, 2010. Cladoceran community responses to

biomanipulation and re-oligotrophication in Lake Vesi-

jarvi, Finland, as inferred from remains in annually lami-

nated sediment. Freshwater Biology 55: 1164–1181.

Ohle, W., 1978. Ebullition of gases from sediment, condition,

and relationship to primary production of lakes. Verhand-

lungen der internationale Vereinigung fur theoretische und

angewandte Limnologie 20: 957–962.

123

Hydrobiologia

Peltonen, H., H. Rita & J. Ruuhijarvi, 1996. Diet and prey

selection of pikeperch (Stizostedion lucioperca (L.)) in

Lake Vesijarvi analysed with a logit model. Annales

Zoologici Fennici 33: 481–487.

Peltonen, H., J. Ruuhijarvi, T. Malinen, J. Horppila, M. Olin & J.

Keto, 1999a. The effects of food-web management on fish

assemblage dynamics in a north temperate lake. Journal of

Fish Biology 55: 54–67.

Peltonen, H., J. Ruuhijarvi, T. Malinen & J. Horppila, 1999b.

Estimation of roach (Rutilus rutilus (L.)) and smelt (Os-

merus eperlanus (L.)) stocks with virtual population anal-

ysis, hydroacoustics and gillnet CPUE. Fisheries Research

44: 25–36.

Penczak, T., M. Molinski, W. Galicka & A. Prejs, 1985. Factors

affecting nutrient budget in lakes of R. Jorka watershed

(Masurian Lakeland, Poland) VII. Input and removal of

nutrients with fish. Ekologia Polska 33: 301–309.

Preece, E. P., B. C. Moore, M. M. Skinner, A. Child & S. Dent,

2019. A review of the biological and chemical effects of

hypolimnetic oxygenation. Lake and Reservoir Manage-

ment 35: 229–246.

Ramcharan, C. W., R. L. France & D. J. McQueen, 1996.

Multiple effects of planktivorous fish on algae through a

pelagic trophic cascade. Canadian Journal of Fisheries and

Aquatic Sciences 53: 2819–2827.

Romare, P. & L. A. Hansson, 2003. A behavioral cascade: top

predator induced behavioral shifts in planktivorous fish and

zooplankton. Limnology and Oceanography 48:

1956–1964.

Ruuhijarvi, J., T. Malinen, P. Ala-Opas & A. Tuomaala, 2005.

Fish stocks of Lake Vesijarvi: from nuisance to flourishing

fishery in 15 years. Verhandlungen der internationale

Vereinigung fur theoretische und angewandte Limnologie

29: 384–389.

Ruuhijarvi, J., T. Malinen, K. Kuoppamaki, P. Ala-Opas & M.

Vinni, 2020. Responses of food web to artificial circulation

in Lake Vesijarvi. Hydrobiologia (this issue).

Salmi, P., I. Malin & K. Salonen, 2014. Pumping of epilimnetic

water into hypolimnion improves oxygen but not neces-

sarily nutrient conditions in a lake recovering from

eutrophication. Inland Waters 4: 425–434.

Salonen, K., M. Pulkkanen, P. Salmi & R. W. Griffiths, 2014.

Interannual variability of circulation under spring ice in a

boreal lake. Limnology and Oceanography 59: 2121–2132.

Sarvala, J., H. Helminen, V. Saarikari, S. Salonen & K. Vuorio,

1998. Relations between planktivorous fish abundance,

zooplankton and phytoplankton in three lakes of differing

productivity. Hydrobiologia 363: 81–95.

Sarvala, J., H. Helminen & J. Karjalainen, 2001. Restoration of

Finnish lakes using fish removal: changes in the chloro-

phyll-phosphorus relationship indicate multiple controlling

mechanisms. Verhandlungen der Internationale Vereini-

gung fur theoretische und angewandte Limnologie 27:

1473–1479.

Sarvala, J., H. Helminen & J. Heikkila, 2020. Invasive sub-

merged macrophytes complicate management of a shallow

boreal lake: a 42-year history of monitoring and restoration

attempts in Littoistenjarvi, SW Finland. Hydrobiologia.

https://doi.org/10.1007/s10750-020-04318-7.

Scheffer, M., S. H. Hosper, M.-L. Meijer, B. Moss & E.

Jeppesen, 1993. Alternative equilibria in shallow lakes.

Trends in Ecology & Evolution 8: 275–279.

Seitzinger, S. P., 1991. The effect of pH on the release of

phosphorus from Potomac Estuary sediments: implications

for blue-green algal blooms. Estuarine Coastal and Shelf

Science 33: 409–418.

Shapiro, J., V. Lamarra & M. Lynch, 1975. Biomanipulation: an

ecosystem approach to lake restoration. In Brezonik, P. L.

& J. F. Fox (eds), Water Quality Management Through

Biological Control. Univ. of Florida, Gainesvill: 85–96.

Sommer, U., F. Sommer, B. Santer, C. Jamieson, M. Boersma,

C. Becker & T. Hansen, 2001. Complementary impact of

copepods and cladocerans on phytoplankton. Ecology

Letters 4: 545–550.

Søndergaard, M., P. Kristensen & E. Jeppesen, 1993. Eight

years of internal phosphorus loading and changes in the

sediment phosphorus profile of Lake Søbygaard, Denmark.

Hydrobiologia 253: 345–356.

Søndergaard, M., E. Jeppesen, T. L. Lauridsen, C. Skov, E.

H. Van Nes, R. Roijackers, E. Lammens & R. Portielje,

2007. Lake restoration: successes, failures and long-term

effects. Journal of Applied Ecology 44: 1095–1105.

Tammeorg, O., T. Mols, J. Niemisto, H. Holmroos & J. Horp-

pila, 2017. The actual role of oxygen deficit in the linkage

of the water quality and benthic phosphorus release:

potential implications for lake restoration. Science of the

Total Environment 599–600: 732–738.

Tarvainen, M., J. Sarvala & H. Helminen, 2002. The role of

phosphorus release by roach (Rutilus rutilus) in the water

quality changes of a biomanipulated lake. Freshwater

Biology 47: 2325–2336.

Urrutia-Cordero, P., M. K. Ekvall & L.-A. Hansson, 2015.

Responses of cyanobacteria to herbivorous zooplankton

across predator regimes: who mows the bloom? Freshwater

Biology 60: 960–972.

Venetvaara, J. & E. Lammi, 1995. Vesijarven kasvillisuuden

nykytila ja viimeaikaiset muutokset (in Finnish with Eng-

lish abstract). In Sammalkorpi, I., J. Keto, T. Kairesalo, E.

Luokkanen, M. Makela, J. Vaariskoski & E. Lammi (Eds),

Lake Vesijarvi Project: Mass Removal of Cyprinids and

Traditional Water Protection. Publications of Water and

Environment Administration – Series A 218: 101–106.

Publisher’s Note Springer Nature remains neutral with

regard to jurisdictional claims in published maps and

institutional affiliations.

123

Hydrobiologia